An integrative approach to identify and experimentally validate environmental variables which affect SCTLD outcomes

Disease outbreaks have caused mass coral mortality on Florida’s Coral Reef (FCR) and continue to threaten the persistence of coral populations. Spatiotemporal variations in disease dynamics suggest environmental conditions influence susceptibility, the probability of contracting disease, and severity, the probability of dying from disease. Understanding these variations may allow us to identify the factors which underpin coral health and predict future disease dynamics. We combined field observations and statistical modelling to identify the environmental conditions that influenced disease dynamics during the SCTLD outbreak, and performed lab experiments under these conditions to understand their effect on immunity in Montastraea cavernosa. 

Disease susceptibility was quantified using data collected during the peak SCTLD outbreak. Disease severity was calculated as the change in M. cavernosa abundance at CREMP and SECREMP sites in the first two years following the outbreak. Environmental predictors were quantified using in situ and satellite data. Disease susceptibility and severity were modelled against these predictors in a two-step process using random forests and generalized linear mixed models. 

Disease susceptibility was most strongly influenced by the interactions between maximum temperature and maximum chlorophyll-a concentration (nutrient proxy) the month prior to the disease survey, and between maximum chlorophyll-a and three-month mean PAR prior to the disease survey. Disease probability was highest when chlorophyll-a concentration exceeded ~6 mg m-3 and maximum temperatures were below 30 °C or when mean PAR and chlorophyll-a concentrations were high. Disease severity had a negative relationship with maximum temperature, such that unless temperatures exceeded 31.08 °C there was an over 50% chance of a colony dying. 

Lab experimentation investigated the impact of temperature and nutrients, the interaction identified as most strongly influencing disease susceptibility, on coral immune response. A crossed design with six treatments reflective of conditions experienced on FCR was used: temperature (high or ambient) and nutrients (none, moderate or high). After one month of environmental manipulation, coral fragments were immune challenged by pathogenic stimuli or placebo to assess immune response. Multivariate analysis revealed strong impacts of temperature, nutrients (ammonia concentration), and the interaction of nutrients and immune challenge. Heat stress largely drove broad suppression of constitutive immunity (peroxidase, phenoloxidase, and antibacterial activity), but increased catalase activity. Corals exposed to moderate levels of ammonia (0.01 mg/1) induced the strongest immune responses (catalase and phenoloxidase activity), but this benefit was lost at high concentrations (0.05 mg/l). 

Our results suggest temperature played the primary role in SCTLD susceptibility and severity and that it strongly influences immune response. Temperatures which likely induced bleaching were related to reduced SCTLD severity, strengthening findings that suggest it initially affected Symbiodiniaceae before causing host tissue loss. However, lab experiments found multiple immune metrics were suppressed at elevated temperatures, while enhanced catalase activity suggests stress within the coral, suggesting further disease outbreaks are likely as ocean temperatures rise. Both methods suggest that under eutrophic conditions immune response is lower and disease susceptibility increases. The experimental eutrophic conditions are experienced on FCR, and our results suggest reducing ammonia in these locations could improve coral immunity and reduce the likelihood of another major disease outbreak